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Single-cell transcriptomic analysis of honeybee brains identifies vitellogenin as caste differentiation-related factor.

ABSTRACT: The honeybee (Apis mellifera) is a well-known eusocial insect. In honeybee colonies, thousands of sterile workers, including nurse and forager bees, perform various tasks within or outside the hive, respectively. The queen is the only fertile female and is responsible for reproduction. The queen and workers share similar genomes but occupy different caste statuses. We established single-cell transcriptomic atlases of brains from queens and worker subcastes and identified five major cell groups: Kenyon, optic lobe, olfactory projection, glial, and hemocyte cells. By dividing Kenyon and glial cells into multiple subtypes based on credible markers, we observed that vitellogenin (vg) was highly expressed in specific glial-cell subtypes in brains of queens. Knockdown of vg at the early larval stage significantly suppressed the development into adult queens. We demonstrate vg expression as a "molecular signature" for the queen caste and suggest involvement of vg in regulating caste differentiation.

SUBMITTER: Zhang W

PROVIDER: S-EPMC9254125 | biostudies-literature | 2022 Jul

REPOSITORIES: biostudies-literature

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Single-cell transcriptomic analysis of honeybee brains identifies vitellogenin as caste differentiation-related factor.

Zhang Wenxin W Wang Liangliang L Zhao Yinjiao Y Wang Yufei Y Chen Chaoyang C Hu Yu Y Zhu Yuanxiang Y Sun Hao H Cheng Ying Y Sun Qinmiao Q Zhang Jian J Chen Dahua D

iScience 20220618 7

The honeybee (<i>Apis mellifera</i>) is a well-known eusocial insect. In honeybee colonies, thousands of sterile workers, including nurse and forager bees, perform various tasks within or outside the hive, respectively. The queen is the only fertile female and is responsible for reproduction. The queen and workers share similar genomes but occupy different caste statuses. We established single-cell transcriptomic atlases of brains from queens and worker subcastes and identified five major cell g ...[more]

PMID: 35800778

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Project description:BackgroundIn honeybees, differential feeding of female larvae promotes the occurrence of two different phenotypes, a queen and a worker, from identical genotypes, through incremental alterations, which affect general growth, and character state alterations that result in the presence or absence of specific structures. Although previous studies revealed a link between incremental alterations and differential expression of physiometabolic genes, the molecular changes accompanying character state alterations remain unknown.ResultsBy using cDNA microarray analyses of >6,000 Apis mellifera ESTs, we found 240 differentially expressed genes (DEGs) between developing queens and workers. Many genes recorded as up-regulated in prospective workers appear to be unique to A. mellifera, suggesting that the workers' developmental pathway involves the participation of novel genes. Workers up-regulate more developmental genes than queens, whereas queens up-regulate a greater proportion of physiometabolic genes, including genes coding for metabolic enzymes and genes whose products are known to regulate the rate of mass-transforming processes and the general growth of the organism (e.g., tor). Many DEGs are likely to be involved in processes favoring the development of caste-biased structures, like brain, legs and ovaries, as well as genes that code for cytoskeleton constituents. Treatment of developing worker larvae with juvenile hormone (JH) revealed 52 JH responsive genes, specifically during the critical period of caste development. Using Gibbs sampling and Expectation Maximization algorithms, we discovered eight overrepresented cis-elements from four gene groups. Graph theory and complex networks concepts were adopted to attain powerful graphical representations of the interrelation between cis-elements and genes and objectively quantify the degree of relationship between these entities.ConclusionWe suggest that clusters of functionally related DEGs are co-regulated during caste development in honeybees. This network of interactions is activated by nutrition-driven stimuli in early larval stages. Our data are consistent with the hypothesis that JH is a key component of the developmental determination of queen-like characters. Finally, we propose a conceptual model of caste differentiation in A. mellifera based on gene-regulatory networks.

Project description:Honeybee (Apis mellifera) exhibits divisions in both morphology and reproduction. The queen is larger in size and fully developed sexually, while the worker bees are smaller in size and nearly infertile. To better understand the specific time and underlying molecular mechanisms of caste differentiation, the proteomic profiles of larvae intended to grow into queen and worker castes were compared at 72 and 120 hours using two dimensional electrophoresis (2-DE), network, enrichment and quantitative PCR analysis. There were significant differences in protein expression between the two larvae castes at 72 and 120 hours, suggesting the queen and the worker larvae have already decided their fate before 72 hours. Specifically, at 72 hours, queen intended larvae over-expressed transketolase, aldehyde reductase, and enolase proteins which are involved in carbohydrate metabolism and energy production, imaginal disc growth factor 4 which is a developmental related protein, long-chain-fatty-acid CoA ligase and proteasome subunit alpha type 5 which metabolize fatty and amino acids, while worker intended larvae over-expressed ATP synthase beta subunit, aldehyde dehydrogenase, thioredoxin peroxidase 1 and peroxiredoxin 2540, lethal (2) 37 and 14-3-3 protein epsilon, fatty acid binding protein, and translational controlled tumor protein. This differential protein expression between the two caste intended larvae was more pronounced at 120 hours, with particular significant differences in proteins associated with carbohydrate metabolism and energy production. Functional enrichment analysis suggests that carbohydrate metabolism and energy production and anti-oxidation proteins play major roles in the formation of caste divergence. The constructed network and validated gene expression identified target proteins for further functional study. This new finding is in contrast to the existing notion that 72 hour old larvae has bipotential and can develop into either queen or worker based on epigenetics and can help us to gain new insight into the time of departure as well as caste trajectory influencing elements at the molecular level.

Project description:Honeybees are very important eusocial insects and are involved in the pollination of many plants. Queen bees and worker bees develop from the same fertilized eggs, and are thus genetically identical despite their substantial behavioural and physiological differences. The mechanism governing developmental differences between worker and queen bees has always attracted much interest. While there are several reports on mRNA expression related to caste differentiation, no systematic investigation of small RNAs has thus far been carried out. Results: Using deep sequencing we systematically profiled small RNA expression in 4th-6th day worker larvae and queen larvae (the critical stages at which the fates of workers and queens are determined), and found that 38 miRNAs were differentially expressed between worker and queen larvae. In addition, 639 mature miRNA candidates were identified in our work for the first time, of which, 526 were expressed only in workers (318) or queens (208). Conclusion: We present the first profile of honeybee small RNAs and explore the mechanism of caste differentiation between worker and queen bees. Caste-specific expression patterns and large discrepancies in small RNA profiles between worker and queen bees indicate that small RNAs may be related to the differential development of worker and queen bee larvae. Results presented here will make a valuable contribution to understanding the caste switch between worker and queen bees. Three healthy 10-frame colonies of ‘Zhenongda No.1’- a high-yielding royal jelly breed of Apis mellifera ligustica , were maintained at the Huajiachi campus of Zhejiang University. In each colony, the queen laid eggs over a period of 24 hours in one empty frame which was subsequently moved to an egg-free super-chamber. After 66 hours (less than 18 hours after hatching), we transferred 150 larvae into queen cups to rear queens in each colony and put the queen cup frames into their corresponding colonies. 40-60 worker larvae and queen larvae were collected from each colony after 4 days (73~90 h after hatching), 5 days (97~114 h after hatching) and 6 days (121~138 h after hatching). The larval samples were collected into 50 ml tubes, immediately frozen in liquid nitrogen and stored at -80C until being used for RNA extraction. After total RNA was extracted and quantified , relative equal amounts of total RNAs from each of the three sampling days were pooled into respectively worker and queen samples, and the fraction of small RNAs less than 30nt long was retained and sequenced on the Illumina/Solexa high-throughput platform (HTP).

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Single-cell transcriptomic analysis of honeybee brains identifies vitellogenin as caste differentiation-related factor.

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Single-cell transcriptomic analysis of honeybee brains identifies vitellogenin as caste differentiation-related factor.

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